A Compact Closed Genome of Orientia tsutsugamushi from Hainan Island, China Provides a TA763_A Reference and Reveals Repeat-Driven Remodeling

Scrub typhus, caused by the obligate intracellular bacterium <i>Orientia tsutsugamushi</i> (<i>O. tsutsugamushi</i>), remains a major public-health concern in the Asia-Pacific region. Genome-wide inference is complicated by extensive repetitive DNA and frequent genome rearrangement. We isolated <i>O. tsutsugamushi</i> HMU_001 from a scrub typhus patient on Hainan Island, China. Intracellular morphology was examined and replication was quantified in endothelial cells. Using long-read sequencing with short-read polishing, we generated a closed circular genome and performed standardized comparative analyses across all available complete <i>O. tsutsugamushi</i> genomes. HMU_001 assembled as a 1,895,724 bp genome and, among the 17 complete genomes analyzed in this study, represented the most compact genome. Repeats comprised 873,550 bp (46.08%) and included 72 RAGE loci (4 relatively complete) and 283 insertion sequences (54 intact). Repeat content varied widely and largely explained genome size differences. A core-gene phylogeny resolved four clades with partial geographic structure, while <i>tsa56</i> genotypes were only partly congruent with it. Genome synteny was generally limited across strains but markedly higher among the closest relatives, consistent with ongoing rearrangement. HMU_001 expands representation of complete <i>O. tsutsugamushi</i> genomes by adding a TA763_A lineage strain from a high-incidence island setting. Comparative analyses support a model in which repeat proliferation and decay drive genome evolution and structural remodeling.